The Olfactory Organs of Diptera

AUTHOR'S .ABSTRACT OF THIS PAPER I~SUED BY THE BIBLIOGRAPHIC UERVICE, JULY 19

THE OLFACTORY ORGANS OF DIPTERA

N. E. McINDOO

Bureau 0.f Entomology, Washington, D. C.

FIFTY-FIVE FIGURES

CONTENTS Introduction and methods...... 457 The olfactory pores...... 460 Disposition of pores in Musca domestica...... 460 a. Pores on legs ...... 460 b. Pores on wings ...... 460 c. Pores on halteres ...... 461 Disposition of pores in other species a. Pores on legs...... c. Pores on halteres...... 464 d. Pores on abnormal species.. . ' . e. Generic, specific, individual, an Structure of pores in Musca domestica...... 471 a. External structure...... 471 b. Internal structure.. ... Structure of pores in other ...... 478 a. External structure...... 478 b. Internal structure ...... 479 The antennal organ ...... Summary...... I,itcrat,ure cited...... 484

INTRODUCTION AND h'IETIIODS The results herein recorded are a continuation of the writer's investigation concerning the morphology of the olfactory pores. Up to date, including the present results, these organs have been carefully studied in Hymenoptera, Coleoptera, Lepidoptera, and Diptera. The chief object of the present investigation is to determine whether the olfactory pores are better adapted ana. tomically than the antennal organs to receive olfactory stirnuli. 457

THE JOURNAL OF COWARATIVE NEUROLOGY, VOL. %, NO. 5 OCPOBER, 1915 458 N. E. McINDOO

The investigators who have performed experiments on flies with mutilated antennae have concluded that these appendages bear the olfactory organs, regardless of whether or not the antennal organs are anatomically fitted to receive olfactory stimuli. Since these investigators failed to study sufficiently the behavior of the insects investigated, it is possible that the responses observed misled them in determining the seat of the olfactory organs. In 1857 Hicks discovered porelike organs on the wings and halteres of fiies, and claims that they are similar in structure and probably have the same function, that of smell. He was able to trace a nerve to each group of organs, the one going to the halter bking the larger. The same author ('59) found these organs in Hippobosca equina and Tipula olerocea, and in 1860 discovered them on the legs of various insects, including Diptera. In the same year Leydig described and figured the same organs on the halteres of Calliphora (Musca) vomitoria and Eristalis tenax. Each one of the foregoing authors was able to trace nerves to these pores, but they could not understand the internal anatomy of them. Graber ('82) described and figured these organs on the wings and halteres of several Diptera, and called them chordotonal organs, because he thought the peripheral ends of the sense cells were sensory chords. Lee ('85) described and figured in detail these structures on the halteres of Calliphora vomitoria, but he, like the preceding authors, failed to understand their internal anatomy. The paper of Weinland ('90) is the most comprehensive one dealing with the sense organs found on the halteres, and as a whole it is the best, although he did not clearly understand the anatomy of these structures. He gives a good review of the literature pertaining to the halteres, and according to him the earliest writers (beginning in 1711) said that these appendages served in maintaining the equilibrium of the insect while flying ; hence the Latin name, halteres and the English translation, balanciers. About a century later experiments proved that flies with amputated halteres could fly, although not as well, THE OLFACTORY ORGANS OF DIPTERA 459 and konsequently the preceding view has long since been abandoned. Another old view was that the halteres aid in respiration Hicks and Lee regarded the structures as olfactory organs, while Leydig and Graber thought they were auditory in function. Weinland determined that the halteres in vibrating rapidly perform a number of different movements, and chiefly for this reason he thinks that the organs borne by them bring about the perception of movements, thereby steering the flight of the insect. He asserts that since the antennae bear the olfactory organs, the organs on the halteres certainly do not perform the same function. Nagel (’94), in commenting on the probable function of the halteres, thinks that the first four preceding views have been abandoned, but, he is a strong advocate of Weinland’s view. The paper of Prashad (’16) seems to be the most recent one concerning the sense organs on the halteres, and this author studied only the halteres of the mosquito, Ochlerotatus pseudo- taeniatus Giles. He evidently did not have access to most of the literature on this subject and consequently has added little knowledge concerning these organs. He thinks that each organ has an external opening and found two scalpel groups of pores on each halter, while the present writer found only one scalpel group on each halter of mosquitoes belonging to other genera. McEwen (’18) has just recently observed the sense organs on the wings of Drosophila ampelophila. He determined “that these organs had nothing to do with the response to light” (pp. 85 to 87), but performed no experiments using odor stimuli. To obtain material for the study of the disposition of the olfactory pores, dried museum specimens were largely used. These specimens were obtained of Messrs. C. T. Greene and C. H. Popenoe through the courtesy of Dr. L. 0. Howard. Mr. Greene is furthermore to be thanked for verifying the identifi- cation of all the species used. Fresh material was fixed in the modified Carnoy’s fluid, and was embedded in celloidin and paraffin. The sections were cut three and five microns in thick- ness, and were stained in Ehrlich’s hematoxylin and eosin. All the drawings were made by the writer and all are original except figures 50 to 55; these represent the antenna1 organs of flies 460 N. E. McINDOO and mosquitoes, and were copied from Hauser, vom Rath, and Nagel. The drawings were made at the base of the microscope with the aid of a camera lucida.

THE OLFACTORY PORES Before making a study of the anatomy of the organs, called the olfactory pores by the writer ('14 a), the dist,ribution and number of them were first investigated.

Disposition of pores in Musca domesticn Owing to an abundance of material and to thc economic im- portance of the house fly, the olfactory pores of this insect have been studied and drawn in detail, and it is hoped that such work will encourage experimentation along practical lines. a. Pores on legs. Seven goups of pores lie on each leg and the disposition of them is as follows: nos. 1 to 4 on the inner surface of the leg (fig. 1) and nos. 5 to 7 on the outer surface; nos. 1,2, and 5 being on the trochanter, nos. 3 and 6 on the femur, and nos. 4 and 7 on the tibia. Nos. 1 and 2, consisting of 5 and 8 pores, respectively, always lie on the anterior margin of the leg, while no. 3, composed of 11 pores, lies on the posterior margin. Nos. 4 and 7, when present, may lie on eit8heror both margins of tthe leg and the number of pores in each group varies from one to three. No. 5, consisting of 3 pores, usually lies near the posterior margin, while no. 6, composed of 1 pore, lies near the anterior margin. b. Pores on wings. Six groups and several scattered pores lie on each wing and the disposition of thcm is as follows: Nos. 8 to 11 and scattered pores a to c lie on the doma1 surface of the wing (fig. 2), while nos. 12 and 13 and the scattered pores d and e lie on the ventral surface. No. 8, consisting of about 24 pores, lies at the proximal end of the propteiygiurn (Pr),while nos. 9 to 13 lie on the subcostal (Sc)vein in about the positions as indicated by the numbers in figure 2. The number of pores in each of these groups varies slightly, but the average number in each is about as follows: no. 9 has 50 pores; no. 10, 12 pores; no. 11, 10 pores: THE OLFACTORY ORGANS OF DIPTERA 461

No. 12, 9 pores, and no. 13, 18 pores. The scattered pores vary considerably in number and position and they are located about as follows: 1 at a on the base of the humeral vein; 2 always present at b on the distal end of the first radial vein; 1 at c on the radiomedial vein; 1 at d on the proximal end of the first radial vein; and 1 at e on the fourth radial vein.

Fig. 1 Portions of legs of house fly (Musca dornestica c?), showing location of groups nos. 1 to 7 of o1f:xtory pores. The drawings at the right represent the inner surface and those at the left the outer surfnce. , AntM and PostM stand for anterior and posterior margins. X 20.

c. Pores on halteres. Five groups and 1 isolated pore lie on the base of each halter (fig. 3); nos. 14 to 16 and trhe isolated pore at f being found on the dorsal surface and nos. 17 and 18 on the ventral surface. The pores lie on plates whose outlines are similar in shape to the contours of t,he groups of pores themselves; 462 N. E. McINDOO hence, the pores in nos. 14 and 18 have been called scalpel organs because each group lies on a plate shaped like a scalpel. No. 15 lies on the basal plate, consequently its pores have been called basal organs. No. 16 lies 011 the anterior end of the basal plate, while no. 17 on the opposite side of the halter lies on the proximal end of t,he scalpel plate; the pores in these two groups are like in structure, and since their structure is like that of those on the wings they have been called Hicks’ organs. In the following pages it is shown that the scalpel and basal organs are unlike in structure and also neither one of these two types is exactly like the Hicks’ organs. The isolated pore at f is found on only about

Fig. 2 Portion of left wing of Musca dornestica ul, showing location of groups nos. 8 to 13 of olfactory pores on propterygium (Pr)and on subcostal vein (Sc) and the scattered pores at points marked a to e. The drawing at the left represents the dorsal surface and the one at the right the ventral surfacp. X 20. one-half of the halteres of the house fly, and it has been called an undetermined type by Weinland. Considering the twenty halteres belonging to five males and five females, the numbers of pores in the groups are as follows: In no. 14 they vary from 74 to 110 with 92 as an average; in no. 15, from 70 to 96 with 88 as an average; in no. 16, from 10 to 11 wit,h almost 11 as an average; in no. 17, from 3 to 8 with 7 as an average, and in no. 18, from 74 to 110 with 93 as an average. THE OLFACTORY ORGANS OF DIPTERA 463

Disposition of pores in other species In making a comparative study of the disposition of the olfactory pores in Diptera, 47 species, belonging to 38 genera and representing 21 families, were used. In most cases only one specimen of each species was employed, and whenever a portion of an appendage or an entire appendage was missing or was badly mutilated in being prepared for study, the supposed number

Fig. 3 Right halter of Musca dornestica 3,showing location of scalpel pores (nos. 14 and 18), basal pores (no. 15), Hicks’ pores (nos. 16 and 17) and the undetermined type (f). The upper drawing represents the dorsal surface and the lower one the ventral surface. The upper margin of each drawing represents the anterior surface and the lower margin the posterior surface. F, one of the folds caused during preparation of halter. X 100. of pores on this portion or entire appendage was regarded the same as the number found on the corresponding portion or entire appendage on the opposite side of the body. Since the pores on only one specimen for each species were counted, the total number of pores recorded cannot be a fair average. Besides this error, there is also another small probable error for each species, because a few of the pores were probably overlooked, and often, as on the tibiae, it was impossible to distinguish the 464 N. E. McINDOO olfactory pores from hair sockets. As a rule, only the legs, wings, and halteres were examined, although in several instances the chitinous parts of the reproductive organs and the mouth parts were also examined, but usually no olfactory pores were seen on them. The sex of the species, except in a few cases, was not determined. a. Pores on legs. The disposition of the pores on the legs is more similar to that of those on the legs of Hymenoptera (Mc- Indoo, '14 b) than to those on the legs of Lepidoptera or Coleop- tera (McIndoo, '15, '17). Pores were found on each trochanter and femur examined, but sometimes none was seen on a tibia and not one was ever observed on a tarsus. The distribution of them is similar to that of the house fly, already described. The total number of them varies considerably, depending on the number of groups present and the size of the species. The groups are usually conspicuous and the one on the femur is quite characteristic; it consists of two or three rows of pores variously arranged, depending on the genus examined. b. Pores on wings. The disposition of the pores on the wings is more similar to that of those on the wings of Lepidoptera than to those on the wings of Hymenoptera or Coleoptera. In Lepi- doptera the pores are well grouped, while in Diptcra they are poorly grouped and consequently not much reliance can be placed upon the number of groups recorded; for this reason the variation in the number of groups need not be discussed. Lepidoptera have more isolated pores than have Diptera, and in the former order they may extend along the full length of the veins, while in Diptera they are never found farther than two-thirds the dis- tance from the base of the wing. The propterygium (fig. 2, Pr.) was often lost during the preparation of the integument, but group No. 8, was usually found on it whenever this part of the wing was present. This is the first time hr this group to be reported. c. Pores 012 hnlteres. As already mentioned on page 462, there are four types of pores on the hnlteres, although the undcterminde type, consisting of large isolated pores, should be callcd isolated Hicks' porcs. The groups of Hicks' pores are seen only with THE OLFACTORY ORGANS OF DlPTERA 465 much difficulty and doubtless many of them were overlooked. The writer is the only observer who has seen a group of them on either side of the halter. Since the number of pores on the halteres has never been tabulated, the following table is presented. A reference to this table will show the minor variations in these pores better than a description of them, therefore only the more important variations ne6d be pointed out. The Hicks’ groups were found on 75 per cent of the halteres; a basal group on each halter, except in one species (no. 2); one or two scalpel groups on each halter; and the undetermined pores on 45 per cent of the halteres examined. One basal group (excepting no. 2) was invariably present on each halter, while two scalpel groups were observed on each halter examined, except in the three mosquitoes (nos. 3 to 5) and two of the wingless forms (nos. 13 and 48); only one scalpel group was seen on each halter of these five species. d. Pores on abnormal species. To determine what effect en- vironmental conditions has had upon the disposition of the 01- factory pores, seven species were selected for this purpose. Table 3 (p. 470) shows to what families they belong and the number of their olfactory pores in comparison with the pores of the normal species. In table 2 they are arranged according to the degree of degeneracy of the wings and halteres and they shall be described accordingly. The sheep tick (45 Melophagus ovinus) is much compressed; has no signs of wings and halteres; its legs are short and the segmcnts are wide; the entire integument is thick and tough. Olfactory pores were found only on the trochanters and femora; their distribution is normal, but their number is reduced. The bat tick (48 Nycteribia bellardii) is also much compressed and has no compound eyes; its wings are totally wanting and its halteres are unusually small. The disposition of the pores on its legs is normal, but on the halteres the pores are comparatively few; the scalpel type being reduced to only one group per halter (table 1). The so-called wingless female of the snow-fly (2 Chionea valga) copulates on the surface of the snow and it seems to be abnormal in four ways; 1) The number of pores on 466 N . E . McINDOO

TABLE 1 Number of organs in the four types of olfactory pores found on the halteres of Diptera . TYPE .

*Nos NO0 *kiz . No . 15 . 'oh1 15 and 17 Baal 14 and 18 d.3 lum- NIIYBER AND NAMES OF SPECIES Hicks' Scalpel ae ?r of 3 ores .. . . . ~ .

TABLE I-Cunlinued

TYPE

___c

'Nos. No. 15 NOS. rota1 15 and 17 14 and 18 NUMBER AND NAMES OF SPECIES Basal num- Hicks' Scalpel ber of pores __ - ~ - - __ Num. ium Num. rTum Num Num ber 01 er o ler 01 er o Ner a ,er o roupr mres roupa mres roup pores - - - 37. Musca domestica 8...... 4 35 2 183 4 387 606 38. Musca domestica 0...... 4 35 2 166 4 350 552 39. Sarcophaga plinthopyga.. , . . , 2 18 2 140 4 316 474 40. Sarcophaga lambens...... 2 32 2 168 4 334 534 41. Sarcophaga helicis...... 4 48 2 186 4 326 564 42. Sarcophaga sp...... 4 36 2 146 4 292 474 7 43. Sarcophaga sp...... 4 34 I 150 4 334 518 44. Olfersia americana 8..... ',.. 2 60 4 242 304 45. Melophagus ovinus 0...... t 46. Lipoptena depressa 8..'..... 2 10 2 68 4 122 200 47. Hippobosca struthinionis 3.. 2 16 2 130 4 304 442 48. Nycteribia bellardii 3...... 2 6 2 36 44 __ - __ - - __ __ 0- 0- 0- 0- 2- 26- 28 - Variation...... J 4 48 2 27 2 4 552 870 __ - - - * These numbers refer to those in figure 3. showing the same types on thc halteres of the house fly. t Halteres totally wanting. the legs is slightly more than might be expected; 2) the wing is nothing more than a little pad, about as long as the base of the halter, but it bears no pores; 3) the halteres seem normal in size, but the pores on them are comparatively few in number, the Hicks' and basal groups being absent; 4) the ovipositor seems to bear 21 small pores, but they are not recorded in the tables. The chitinous parts of the genital organs of all the abnormal species and of a few of the normal species were examined, but no olfactory pores were observed on them except as above stated. The so-called wingless female phorid (13 Pulicifora borinquensis) is the smallest specimen examined. The wing is padlike, about the size of the halter and it bears 7 pores. The number of pores on the halter appears to be reduced. The deer tick (46 Lipop- tena depressa) has vestigial wings which are unusually thick 468 N. E. McINDOO at the base. The number of pores on them is greatly reduced. The two remaining parasitic species, the fowl tick (44 Olfersia americana) and the ostrich tick (47 Hippobosca struthinionis), are winged and apparently are normal, unless one considers the number of their pores slightly reduced.

TABLE 2 Number of olfactory pores found on abnormal species

NUMBER OF PORES ON Total NUMBER AND NAME OF SPECIES number of Legs I Wings I Halterea pores .. .. 45. Melophagus ovinus 0...... I62 A E 162 48. Nycteribia bellardii 3... , ...... , . , .. 178 A F44 222 2. Chionea valga O...... , . , ...... , , . 391 B 28 419 13. Pulicifora borinquensis 9 ...... 168 C14 140 322 46. Lipoptena dcpressa 8.... , ...... , , , . 144 D75 200 419 44. Olfersia americana. c?. .... ‘. .... , . , .. 168 154 304 626 47. Hippobosca struthinionis 8.. , , , , ... 180 167 442 789 -______144- 00- 00- 162- Variation...... 391 167 442 789

The following is an explanation of letters A to F in the above table: A, totally wingless; B, wing about as long as base of halter; C, wing about size of halter; D, wing much reduced, about same length as that of the short tarsus; E, halteres tntnlly wanting; and F, halteres unusually small and peduncles threadlike. e. Generic, specific, individual, and sexual variafions. As already stated, the variations between the olfactory pores of Hymenoptera, Coleoptera, Lepidoptera, and Diptera are large and in regard to both disposition and structure of the pores they are characteristic for each order. The variations among the families depend upon the families compared; for example, the disposition of the pores in Tipulidae and Muscidae is very different, but in Muscidae and Sarcophagidae only slightly different. The generic characteristics are slight variations in the disposition of the pores, while the specific variations are based almost solely upon the total number of pores present. The individual and sexual variations are distinguishable only by comparing the total number of pores present. h reference to tables 1 and 3 shows that the variations found pcrtain to the number of groups on the halteres and to the variations in number of pores on the legs, wings, and halteres. Exclud- THE OLFACTORY ORGANS OF DIPTERA 469 ing the wingless forms (nos. 13 and 48), the mosquitoes (nos. 3 to 5) differ from all the other Diptera examined in that each halter bears only one scalpel group instead of two. While the legs and wings of these mosquitoes are long and slender, the halteres are short and stout; relative to the other species examined, the reverse is generally true. The number of pores on the halteres of mosquitoes is considerably less than the average number on the halteres of flies, but they appear to be considerably larger. Tipulidae is the only family which bears more pores on the legs than on either the wings or halteres. As a rule, the smaller species bear fewer pores than the largar ones, but there are many exceptions; for example, Tritoxa flexa (no. 16) is one of the largest specimens examined, yet its total number of pores is among the lowest recorded. Among the genera the total number of pores may vary slightly, as in the mosquitoes (nos. 3 to 5) and in Anthomyidae, or considerably, as in Myce- tophilidae and Empididae; but among the species the total number usually varies only slightly, as in nos. 24 and 25, 30 and 31, 34 and 35, but occasionally a larger variation may be found, as in nos. 21 to 23 and 39 to 43. The olfactory pores on five fern-ales and five males of Musca domestica were carefully counted to determine the individual and sexual variations. For the females the number of pores on the legs vary from 165 to 175 with 186 as an awrage; on the wings, from 219 to 274 with 252 as an average; on the halteres, from 530 to 570 with 552 as an average. For the males the number of pores on the legs vary from 168 to 180 with 172 as an average; on the wings, from 232 to 257 with 248 as an average; on the halteres, from 564 to 625 with 606 as an average. Thus, as an average a female bears 972 pores and a male 1026 pores. The mouth parts and antennae of many specimens were examined, but ~o olfactory pores were seen on them. Other parts of the integuments besides those discussed were also often examined, although no olfactory pores were found on them, except on the ovipositor already mentioned (p. 467) and occasionally two or thrce pores on the thorax near t,he base of the wing. These were not carefully recorded and do no-t appear in the tables. 470 N . E . McINDOO

TABLE 3 Number of olfactory pores on legs. wings. and halteres of Diptera . IUMBER OF PORES 'otal ON ium- FAMILY NUMBER AND NAME OF SPECIES .. ~ er of Hal- mrea ,egs Vingi ;ere8 .. 580 252 230 862 Tipulidae ...... I 1. Tipula sp...... 1 2 . Chionea valga 0 Harr ...... 391 B* 28 419 3 . Culex pipiens L ...... 208 170 286 664 Culicidae ...... ! 4 . Aedes vexans Meig...... 194 192 298 684 I 5 . Corethra cinctipes Coq ...... 120 160 298 678 6 Mycetophila punctata Meig 225 343 350 918 Mycetophilidae . . . 7 . Sciaria inconstans Fitch., . . 160 138 330 628 Stratiomyidae.... 8. Macrosargus decorus Say... 272 408 870 550 186 60 282 Empididae ...... 9 . Tachydromia sp...... 528 { 10 . Rhamphomyia abdita Coq ...... 148 192 536 876 Dolichopodidae . . 11. Psilopus sp ...... 168 163 588 919 12. Aphiochaeta sp...... 159 74 278 511 Phoridae ...... 1 13. Pulicifora boringuensis 0 Wheele 168 214 140 322 Micropezidae ..... 14. Calobata antennipes Say., ...... 138 161 430 729 Sepsidae ...... 15. Piophila casei L ...... 124 154 389 667 16. Tritoxa flexa Wied ...... 90 111 272 473 17. Anacampta latiuscuta Loew ...... 151 222 485 858 Ortalidae ...... 18. Euxesta notata Wied ...... 166 184 434 784 19. Dacus cucurbitae Coq ...... 182 192 514 888 Agrompidae..... 1 20 . Milichiella lacteipennis Loew .... 128 124 47 1 723 I 21 . Drosophila busckii Coq ...... 160 98 288 546 Drosophilidae ... { 22 . Drosophila amoena Loew ...... 173 110 324 607 23 . Drosophila funebris Fabr ...... 180 117 358 655 I 24 . Paralimna decipier Loew ...... 168 138 309 615 Ephydridae..... { 25 . Paralimna appendiculata Loew . . 173 126 342 641 26 . Ephydra gracilis Pack ...... 164 183 306 653 Chloropidae., .... 27 . Chlorops coxendix Fitch. 177 138 256 571 Sciomyzidae ..... 28 . Tetanocera plumos Loew ...... 174 202 588 964 Helompzidae ..... 29 . Helomyzn hcta Walk ...... 172 197 522 891 30 . Scatophaga stercoraria L ...... 170 214 470 854 Scotophagidae . . 1 31. Scatophaga surcata Say ...... 173 208 472 853 1 32 . Homalomyia canicularis L ...... 195 198 492 885 33 . Hylemyia simpla Coq ...... 178 241 466 885 Ant honiyidae ... { 34 . Phorbia brassicae Bouche., ...... 174 236 502 912 35. Phorbia fussiceps Zett .... 177 240 502 919 36 . Coenosia sp...... 178 223 404 805 37 Musca domestica 3 L ...... 172 248 606 026 Muscidae ...... < . 38 . Muscn domestica 0 L 168 252 552 972 .. THE OLFACTORY ORGANS OF DIPTERA 47 1

TABLE &Continued __ 1 NUMBER OFPORES Total n um- FAMILY NUMBER AND NAME OF SPECIES ber of I- I- pores - __ 39. Sarcophaga plinthopyga Wied ..... 174 198 474 846 40. Sarcophaga lambens Wied ...... 170 204 534 908 Sarcophagidae. . 41. Sarcophaga helicis Towns.. .. ‘. ... 179 218 564 961 1 42. Sarcophaga sp...... 180 848 I 43. Sarcophaga sp...... 186 906 44. Olfersia americana $ Leach...... 168 626 45. Melophagus ovinus 0 Hippoboscidae.. L...... 162 162 I 46. Lipoptena depressa $ Say...... 144 419 I 47. Hippobosca struthinionis 8 Jansen 180 167 442 789 Nycteribiidae.. .. 48. Nycteribia bellardii 3 Rondani.. 178 A F44 222 - 90- Variation ...... f 162- 11 391 .550

~ ~~ - * For explanation of letters A to F, see p. 468.

Structure of pores in Musca domestica The preceding pages deal with the disposition of the olfactory pores, and now a discussion of their anatomy will be given. a. External structure. As already stated, the pores in groups nos. 16 and 17 on the halteres (fig. 3) have been called Hicks’ organs, and since their structure is like that of those on the legs and wings, all of these pores may be regarded as belonging to the Hicks’ type. Since their anatomy does not differ materially from that of those in the other orders of insects, discussed in other papers by the writer, a reference to figures 4 to 15 may suffice at this place. Under a high-power lens the scalpel groups (nos. 14 and 18) and t,he basal group (no. 15) look somewhat as shown in figures 16 and 17. They may be compared with the Hicks’ type (nos. 16 and 17). It is to be noted that the scalpel group no. 14 consists of 11 rows and no. 18 of 10 rows. From a superficial view the rows appear to be flat, but sections will show that the pores are linked together and stand in ridges, projecting far above the surrounding integument. The summit of each‘ridge is beautifully sculptured, and a row of stout hairs (fig. 16, Hrl) 472 N. E. McINDOO arises between each two rows of pores. These rows of hairs are only prolongations of the chitin and therefore should be called pseudohairs; their only function is probably to protect the rows of pores. The apertures (PorAp) of the pores are invariably long, narrow slits, while sculptured markings replace the pore walls and pore borders in the Hicks' type. The two halves

Figs. 4 to 15 Extcrnal view of olfwtory pores in Musra domestica 8,showing variation in size. Fig. 4, groups nos. 1 and 2 (fig. I);fig. 5, group no. 3; fig. 6, group no. 4; fig. 7, group no. -5; fig. 8, group no. 6;fig. 9, group no. 8 (fig. 2); fig. 10, group no. 9; fig. 11, 10 of 12 pores in group no. 10; fig. 12,9 of 10 pores in group no. 11 ; fig. 13, group no. 12; fig. 14, 6 of 18 pores in group no. 13; fig. 15, scattered pores at b. X 500.

(PorR),surrounding the aperture, are similar in position to the pore wall, but do not correspond to it; this structure may be called the pore ridge. The portion, markcd PorL, may be called the pore link, because it unites the pore ridges; in position it is similar to the pore b&der, but it is quite different in structure. The structure of thc basal type of porcs is similar to that of the Hicks' type, excepting pore borders are not present and a row of THE OLFACTORY ORGANS OF DIPTERA 473 pseudohairs arises between each two rows of pores. Each basal group consists of about eight rows of pores. which are usually smaller than the scalpel pores; the pseudohairs in this group are also smaller than those in the scalpel group. The Hicks’ pores are never protected by pseudohairs.

Figs. 16 and 17 External view of scalpel pores (nos. 14 and 18), basal pores (no. 15), Hicks’ pores (nos. 16 and 17), and the undetermined type (f) on base of right halter of Musca domestica 3 (fig. 3). All of the pseudohairs (Hr*)in group no. 15 are represented, but only a few of those in groups nos. 14 and 18 are shown, the bases of the remainder being represented by black dok. x 500.

b. Internal structure. As in Lepidoptera, the olfactory pores of Diptera may be called dome-shaped structures. All of the pores on the legs (fig. 18) and most of those on the wings (fig. 19) are typical dome-shaped structures, while the remainder on the wings (figs. 20 and 21) and all of those on the halteres (figs. 23 to 27) are modifications of the typical structure. It will be noted that the internal structure of each type of pore is identical to that of any other type and it is also similar to that of the

THE JOURNAL OF COMPAR~TIYENEUROLOGY, YOL. 29. NO. 5 474 N. E. McINDOO olfactory pores in other orders of insects; therefore, it is the external structure that really determines the various types. A hypodermal strand (figs. 23, 26, and 28, HypS), running from the hypodermis (fig. 25, Hyp) to the chitinous cone (fig. 26, Con), is always present. In this strand may be observed the

Figs. 18 to 28 Sections showing internal anatomy of olfactory pores of Musca domestica. Fig. 18, from trochanter; figs. 19 to 21, 3 variations on wing; fig. 22, portion of cross-section of wing (X 500); fig. 23, largest Hicks' pores; fig. 24, smallest. and fig. 25, largest basal pores, both rows being cut lengthwise; fig. 26,4 rows of largest scalpel pores cut crosswise and 1 cut lengthwise; fig. 27, a row of smallest scalpel pores cut lengthwise; and fig. 28, from an oblique section of a scalpel row of porcs, only their external view and nervous connection having been drawn. The sense fiber (SF) and hypodermal stmnd (HypS) are taken from a deeper focus. Attention is called to the sense fiber ending at the center of the pore apcrture. Con, chitinous cone; HrI, pseudohair; Hyp, hypodermis; AT, nerve; PorAp, pore aperture; PorL, pore link; PorR, pore ridge; SC, sense cell, and Tr. trachea. X 1000.

sense fiber (figs. 23, 25, and 28, SF), but it is easily overlooked owing to the minute size of these organs. The sense cells in the legs arid wings (fig. 22, SC) are spindle-shaped as usual, but in the hztltcres (fig. 25, SC) they are more than spindle-shaped and assume almost a spherical shape (fig. 29, SC). A pore aperture (figs. 19 and 26, PorAp) was seen only occasionally THE OLFACTORY ORGANS OF DIPTERA 475 and then never distinctly; it would never have been regarded as an opening had not the writor scen many good examples of it in the olfactory pores of other insects. These pores are the smallest ones ever examined by the writer, and this fact easily explains why other observers have never seen the pore apertures. The sections were studied under a magnification of 1900 diameters, and with the aid of a camera lucida the drawings made represent a magnification of 3000 diameters before reduction; and they were reduced to 1000 diameters. As already stated, the pores on the legs, wings and groups nos. 16 and 17 on the halteres belong to the Hicks’ type, while group no. 15 belongs to the basal type and nos. 14 and 18 to the scalpel type. A glance at figures 19 to 25 shows that the structure of the basal type (figs. 24 and 25) is like that of the Hicks’ type (figs. 20 and 23)’ and the only difference (not shown in these figures) between these two types is that a row of pseudohairs (fig. 16) lies between each two rows of pores in the basal group. Pseudohairs (figs. 19 and 20, Hrl) also protect some of the pores on the wings, but they are never arranged in rows as they are on the halteres. The size of the pores in any type varies considerably. This is shown by comparing the smallest and largest basal pores (figs. 24 and 25) and the largest and smallest scalpel pores (figs. 26 and 27). The scalpel type differs from the other types in the following three particulars: 1) The domes lie totally above the surrounding chitin; 2) the bottoms of the domes are considerably constricted, while in the basal and Hicks’ types on the halteres the domes are projected about one-half their height above the surrounding integument and their bases are constricted little or not at all, and 3) the tops of the domes are beautifully sculptured and assume a more or less flat surface. One pore (fig. 21) on the wing, resembling a scalpel pore, was found, while several (fig. 20) on t8hewing are identical to those in the Hicks’ and basal groups on the halteres. Sections passing longitudinally through the rows of basal pores show the pores as drawn in figures 25 and 29 (BPorl), while sections passing transversely through the rows show the pores as 476 N. E. McTNDOO drawn in figure 29 (BPorz). Figure 26 represents a section passing transversely through four rows and longitudinally through one row of scalpel pores. In the latter pore, as well as in figures 27, 28, and 29 (SPorJ, the pore ri'dge (PorR) and pore link (YorL) can be identified. Figure 29 represents an oblique longitudinal section through the base of the halter in the direction of AA in figure 3. The large nerve (N) is very conspicuous; it spreads out, fanlike and connects with the masses of sense cells

Fig. 29 Longitudinal section (.$ diagrammatic), cut in dircction of linc Ad in figure 3, through hase of halter of Musca domestics, showing internal anatomy, scalpel pores (nos. 14 and 18), basal pores (no. 15) :tnd Hicks' pores (no. 16). The chordotonnl organ (ChO) is only in its approximate position and was copied from Lee ('85). One row each of basal pores (BPoil) and scalpel pores (SPorl) cut lengt,hwise, and 3 rows of basal pores (BiPor,) and 5 TOWS of scalpel porcs (no. 18) were cut crosswise. Ph, internal view of chitin; Ch,, external view of chitin; Icf, muscle; N, nerve; SC, sense cell, and Tr, trachea. X 500.

(SC). A trachea (Tr), muscles (144) and a chordotonal organ (ChO) are also present. Both Lee and Weinland have studied tJhe chorodotonal organ, but the present writer has paid little attention to it, hoping later to make a special study of this type of sense organ. In figure 29 it is represented in only its approximate position as drawn by Lee. Figures 30 and 31 are scheniatic drawings of a portion of a row in a scalpel group, showing the pores both in perspective and in THE OLFACTORY ORGANS OF DIPTERA 477 section. In figure 30 the row was cut crosswise, passing longitudinally through the slitlike aperture, whereas in figure 31 the row was cut lengthwise, passing transversely through the slitlike aperture. Figure 32 is a drawing, showing a portion of the base of the halter in perspective and in section, it was cu't crosswise in the direction of line BB in figure 3. The muscle (M)and chordotonal organ (ChO) are drawn in only their approximate positions as represented by Weinland ; their points of attachments are incor- rect. The scalpel pores (nos. 14 and 18) and a few basal pores (no. 15), shown both in perspective and in section, lie on

Figs. 30 and 31 Schematic drawings of a portion of a scalpel row on halter of Musca domestica, showing the row in perspective and in section. In figure 30, the row was cut crosswise, longitudinally through the slitlike aperture, while in figure 31 the row was cut lengthwise. The nerve (N)is drawn in perspective, and strong pseudohairs (Hr') bend over the pores, protecting them well. curved plates, and it is noted that the surface of the base of the halter is very rough, being made up of minute hills and hollows. In Weinland's drawings it is noted that the nerve does not run beyond the olfactory pores on the halter, but the trachea runs into the peduncle and stops there. A cross-section of the knob of a halter somewhat resembles a double convex lens; it contains masses of cells which are certainly not sensory, but probably they are the remains of the early hypodermis. The surfaces of the knobs of prepared halteres bear a few true hairs, and they are generally smooth excepting the folds (fig. 3, F), caused by pre- paring the specimens. 47% N. E. McINDOO

Structure of pores in other species Since the structure of the pores in the house fly has been described in detail, only the more important variations concerning the structure of the pores in other Diptera will be mentioned and attention will be called to the various figures. a. External structure. On the legs of one or two specimens the pore walls are diamond-shaped instead of being round and oblong,

Fig. 32 Portion of base of right halter of Musca domestica, cut across in direction of line BB in figure 3, showing halter, scalpcl pores (nos. 14 and 18), and 7 basal pores (no. 15) in perspective and in section. The chordotonal organ (ChO) and muscle (M)were copied from Wcinland ('90) and were drawn in only their approximate positions. and the pore apertures in several instances are long, more or less slit-shaped, and resemble the slits in the lyriform organs of spiders (McIndoo, '11); such is particularly true on the trochanters of Tipula (fig. 33). The pores on the tibiae of Sarco- phags (fig. 34) are very large and striking. The pore wall is surrounded by three areas of differently colored chitin; the inner one is real light in color; the middle one is a little darker, and the outer one, having a soft appearance, is still darker. THE OLFACTORY ORGANS OF DIPTERA 479

b. Internal structure. A reference to figures 35 to 49 shows that the size of the pores usually varies according to the size of the insect studied; thus the average size of the pores in the robber fly (figs. 39 to 43) is greater than that of the pores in the flesh fly (figs. 44 to 49), although the pores on the halters of both flies are about equal in size. While the pores on the legs are always dome-shaped, many of those on the wings (figs. 42 and 46) and a few on the halteres (fig. 47) are not dome-shaped. Many of those on the wings (fig. 45) of Sarcophaga project far above the surrounding chitin and their tops slightly resemble those of the scalpel pores on the halteres. A study of these pores shows a complete series of variations, ranging from the Hicks’ type to the scalpel type, and perhaps each type is still in the trans-

Figs. 33 and 34 External views of olfactory pores of other flies. Fig. 33, a group from trochanter. of Tipula, showing slitlikc pore apertures, and fig. 34, a group from tibia of Sarcophaga plinthopyga, showing 3 areas of chitin around pore wall. X 500. itional stage. Morphologically the scalpel type is the most highly developed, but physiologically it is probably little or no better developed than any other type of pores. All of these results indicate that while the hind wings of Diptera have been gradually reduced in size, consequently gradually diminishing their flying ability, their sensory function has been grcatly increased, and now they bear the highest type of olfactory pore yet found. The latter statemcnt is supported by the fact that in Hymenoptera, the hind wings bear about one- half as many pores as do the front wings; in Lepidoptera the hind wings do not bear quite as many pores as do the front wings, while in Diptera the halteres bear about as many pores as do the wings and legs combined, or close to one-half the total number of pores found. 480 N. E. McINDOO

Figs. 35 to 49 Sections showing variations in internal anatomy oE olfactory pores of other flies. Figs. 35 to 38, from crane fly (Brachypremna dispellens Walk.); fig. 35, from trochanter; fig. 36, from wing; and figs. 37 and 38, from halter, fig. 37 being basal type and fig. 38 being scalpel type. Figs. 39 to 43, from robber fly (Erax mtuans L.); fig. 39, from trochanter; fig. 40, from femur; figs. 41 and 42, from wing, and fig. 43, scalpel type from halter. Figs. 44 to 49, from flesh fly (Sarcophaga sp.); fig. 44, from trochanter; figs. 45 and 46, from wing, and figs. 47 to 49, from halter. X 1000. THE OLFACTORY ORGANS OF DIPTERA 481

THE ANTENNAL ORGANS Several investigators have studied the morphology of the antennal organs in Diptera, but since certain drawings of Hauser ('80), vom Rath ('88), and Nagel ('94) best illustrate the various types of antennal organs, the following discussion will be taken only from these three works. The antennae of Diptera are usually short, generally consisting of only a few segments, which bear so-called olfactory pits.

Figs. 50 to 55. Structure of antennal organs of Diptera; figs. 50 to 52, copied from Hauser ('SO); figs. 53 and 54, from vom Roth ('88); and fig. 55, from Nagel ('94). Fig. 50, longitudinal section through third or last antennal segment of Cyrtoneura stabulans Fll., showing internal anatomy of segment and the compound olfactory pits (C) in section. X 75. The tip of the segment is not aec- tioned, thus showing the simple (A)and compound olfactory pits (B)from a superficial view. Fig. 51, section of a simple olfactory pit, and fig. 52, part of a section of a compound olfactory pit; X 750. Fig. 53, section of simple olfactory pit with projecting hair; X 150. Fig. 54, section of compound olfactoty pit on palpus; X 100. Fig. 55,2 olfactory hairs (Hr)on antenna of a mosquito (Culex pipiens 3); x 500.

Not all of the segments bear such pits, but the distal or last one is usually well provided with them. Sometimes, however, olfactory pits are never present on any segment, as in the mosquitoes. The olfactory pits are divided into simple and com- 482 N. E. McINDOO

pound ones. From a superficial view, a siinple pit looks like a small circle (fig. 50, a) with a dot at its center, while a compound pit resembles a large circle (3)which contains radiating lines and two or more dots. Sections through these pits show that a single hair (fig. 51, Br) arises from the bottom of a simple pit and two or more hairs (fig. 52, Hr) from the bottom of a compound pit (fig. 50, C). The mouth and sides of each pit are well protected by pseudohairs (Hrl). A sense cell (SC') lies directly beneath each sense hair and a nerve fiber runs from each sense cell to the nerve (figs. 50 and 52, N). An idea of hmv well the distal segment is innervated may be had by looking at figure 50. Sometimes the hair in a siinple pit projects out of the mouth of the pit (fig. 53), indica,ting that the primary function of such a hair is that of touch. All types of transitional forms of simple and compound pits have been found, and besides being present on the antennae, the compound pits are sometimes found on the palpi (fig. 54). hIosquitoes do not, secni to have olfactory pits; Nagel has found two types of hairs on their antennae, and he calls the short, stout ones (fig. 55, Hr) olfactory organs. A ma,lc mosquito has only a few of thcsc hairs, while a fcmalc has many. All flies seem to have olfactory pits, but some of them do not have the compound ones, ond a fcw of the latter flies bear only one simple pit on each mtcnnzl segment.

strnmI.mY The disposition of the olfactory porcs on the legs of Diptera is more similar to that of those on t,he lcgs cf Hymenoptera than to those on the legs of Lepidoptera or Coleoptera, but those on the wings of Diptera are more similar to those on the wings of Lepidoptera than to those on the wings of the other two orders. The disposition of the pores on the halteres is entirely different from that of those on the hind wings of the other orders examined. In Hymenoptera the hind wings bear about one-half as many pores as do the front wings; in Lepidoptera the hind wings do not bear quite as many pores as do the front, wings; while in Diptera the halteres bear almost one-half the total number of pores found. Excluding the abnormal forms, the total number of THE OLFACTORY ORGANS OF DIPTERA 483 pores found in the four orders examined varies as follows: For Hymenoptera, from 463 to 2608 with 1286 pores as an average; for Lepidoptera, from 514 to 1422 with 850 pores as an average; for Diptera, from 473 to 1550 with 772 as an average; and for Coleoptera, from 273 to 1268 with 724 pores as an average. As in Lepidoptera, the olfactory pores of Diptera are dome- shaped and their internal anatomy is very similar to that of those in the other three orders, but the sense cells in the halteres are more spherical than usual. For description the pores have been divided into four types as follo-ws: The Hicks’ type includes all of khose on the legs, wings, and a few of those on the bases of the halteres. This type also includes all of those found in the other three orders examined. The other three types are found on the bases of the halteres. The undetermined type really belongs to the Hicks’ type, whilc the basal type is very similar to the Hicks’ type; nevertheless, the basal and scalpel types are quite unique and are found only on the halteres. While the basal pores stand in rows resembling the shape of mountain ranges, each row of the scalpel pores may be likened to an inverted urn-shaped ridge whose summit is more or less flat and is beautifully sculptured. Deep depressions lie between the rows in each type and a row of strong, protective pseudohairs stands in each depression. Morphologically, the scalpel type is the most highly developed, but physi?logically it is probably little or no better developed than any other type of pore. This study indicates that while the hind wings of Diptera have been gradually reduced in size, consequently diminishing their flying ability, their sensory function has been greatly increased. Compared with the antennal organs, the olfactory pores are better adapted anatomically to receive olfactory stimuli, because the peripheral ends of their sense fibers come in direct contact with the external air, while those in the antennal organs are cov- ered with hard chitin. 484 N. E. McINDOO

LITERATURE CITED

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